AMPHIBIANS. Yuan Wang and Ke-qin Gao
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1 Wang Y, Gao K Q, Amphibians. In: Chang M M, Chen P J, Wang Y Q, Wang Y (eds.), The Jehol Biota: The Emergence of Feathered Dinosaurs, Beaked Birds, and Flowering Plants. Shanghai: Shanghai Scientific & Techinial Publishers. 76~85. AMPHIBIANS Yuan Wang and Ke-qin Gao Amphibians ( double life in Greek) are a class of primitive tetrapods (vertebrates with four limbs) that spend at least part of their lives in water and part on land, although some are entirely aquatic or terrestrial. Amphibians provide a biological link between fishes and the true land-living vertebrates, as they are the first group of tetrapods that invaded the land some 370 million years ago. Living amphibians are classified in the Subclass Lissamphibia (with their closely related ancestors in fossil forms). They include not only the familiar forms such as the frogs and toads (Order Anura), salamanders and newts (Order Urodela), but also the less familiar forms such as the limbless caecilians (Order Gymnophiona). Extinct archaic amphibians include labyrinthodonts and lepospondyls that flourished in the Late Paleozoic, from either of which the ancestral stocks of the living amphibians may have evolved. Compared with other vertebrate groups, amphibians, especially the lissamphibians (having thin and fragile bones unfitted for fossilization), are generally less well documented in the fossil record. This is especially, and painfully, true of the Mesozoic Era, during which important events of origin and early diversification of modern amphibians took place. Therefore, discoveries of any lissamphibian fossils of this time are usually newsworthy, if not outright sensational. In the past few years, many well-preserved specimens of lissamphibians were recovered from the Mesozoic beds in western Liaoning, northern Hebei and southeastern Inner Mongolia in China. Most of the fossils are important components of the Jehol Biota that flourished in East Asia about 130~110 million years ago. The recovered fossils constitute a diverse lissamphibian fauna in the late Mesozoic of Asia, and provide crucial information on understanding the biogeographic evolution of early salamanders and frogs of modern amphibian affinities. Before these discoveries, fossil amphibians from China were rather limited in both quantity and taxonomic diversity. Prior to 1998, all the known fossils were the Cenozoic in age (early Miocene to middle Pleistocene), totaling ten species of five genera from five major localities in northern China. Since then, new findings from northeastern China have added nearly as many species of the rare Mesozoic lissamphibians to the Chinese record. The fossils include several hundred well-preserved skeletons, some with clear impressions of soft parts such as eyes, gills, and skins. They also include the earliest known record of several taxonomic groups. These incredible finds have not only rejuvenated amphibian paleontology but also drawn a worldwide attention beyond the scientific community. Frogs are tailless amphibians classified in the order Anura (belonging to the superorder Salientia, which also includes the primitive proanurans). They have unusual body structures that are specialized for jumping. Such structures include a rodlike urostyle formed by fusion of tail vertebrae and the greatly elongated hind limbs with highly modified tarsal elements. The earliest
2 fossil representatives of Salientia were from the Early Triassic of Madagascar and Poland. After a long time evolution, now the order Anura includes some 4,800 living species with a global distribution except for extreme northern latitudes, Antarctica, and most oceanic islands. The fossil frogs known from the Liaoning beds include several archaic forms that documented an important diversification of anurans during the Early Cretaceous time in the area. One of the frogs known from Liaoning is Callobatrachus sanyanensis (Fig. 104, 105), named and described on the basis of a nearly complete skeleton from the Sihetun site. The fossil beds yielded a radiometric date of 125 million years BP, indicating the Early Cretaceous age of the fossil. Taxonomic studies have revealed that Callobatrachus sanyanensis is a primitive member of the Discoglossidae, a basal family group of the living anurans. Callobatrachus is basal (or primitive) in having nine opisthocoelous presacral vertebrae, differing from eight in other discoglossids. It further differs from other members of the family in the combination of the following characters: lacking a dorsal protuberance but having a weak dorsal crest on ilium; having bicondylar sacro-urostylar articulation; lacking dermal sculptures on skull roof, and having anteriorly expanded sacral diapophysis. Living discoglossids in China include five species in a single genus Bombina, with Bombina orientalis popularly known as the oriental fire-bellied toad (Fig. 106). Before the discovery of Callobatrachus, no discoglossid fossils were known in the same range of the extant group in East Asia. Consequently, Callobatrachus represents the first discoglossid frog known from China, and the earliest fossil record of the group from Asia. Mesophryne beipiaoensis (Fig. 107) is another Mesozoic frog reported from the Liaoning beds. It is represented by a nearly complete skeleton split on part and counterpart of a shale slab. It has obviously different osteological structures from Callobatrachus, including the presence of procoelous presacrals and greatly shortened vertebral column. It is worth noting here that Mesophryne also has nine presacrals, albeit having a short vertebral column. The number of presacral vertebrae is among the few crucially significant anatomical features in the evolution of frogs. In the earliest known frog, Triadobatrachus (a proanuran) of the Early Triassic of Madagascar, this number is as many as 14; Vieraella, an Early Jurassic frog from Argentina, has ten presacrals. Nine presacrals can be found in the Middle to Late Jurassic Argentine frog Notobatrachus, as well as in the aforementioned two Early Cretaceous Chinese taxa. This number is eight or fewer in all living frogs, except for two very primitive forms, Ascaphus (North American tailed frogs) and Leiopelma (New Zealand frogs), both having nine presacrals. Thus, the decrease in presacral number has been recognized as an obvious trend in the frog evolution. In addition to its large presacral number, Mesophryne also has primitive features such as the presence of free ribs on anterior three presacrals, and the retaining of an intermedium bone in the carpal region. Thus, it is not surprising that a recent phylogenetic study has recognized it as a distinct clade of basal anurans (Fig. 108). Liaobatrachus grabaui is the first Mesozoic frog described from the Liaoning beds; however, its systematic position is still questionable at present. Liaobatrachus grabaui was named and briefly described in early 1998 based on an incomplete skeleton with a disarticulated and poorly preserved skull. It has a snout-pelvic length of about 75 mm, intermediate between Callobatrachus sanyanensis (94 mm) and Mesophryne beipiaoensis (71.3 mm). The taxonomic status of this animal remains to be investigated, as the referral of it to the family Pelobatidae (by
3 the original researchers) was based on several characters in question, such as the presence of procoelous presacrals and the lack of free ribs, which cannot be confirmed due to poor preservation. Salamanders are tailed amphibians classified in the order Urodela (belonging to the superorder Caudata, which also includes some primitive non-urodeles). In the past few years, several hundreds of salamander fossils have been found from several fossil beds in northern China. Some were recovered from the Fengshan fossil bed in northern Hebei Province, and the Jiufotang Formation in western Liaoning. These strata can be included in the Jehol Group (sensu lato) that has yielded the Jehol Biota. Some other fossils were recovered from the Daohugou locality of southeastern Inner Mongolia, the strata older in age (refer to Chapter 2 for stratigraphic information). The discovery of Mesozoic salamanders from China has special implications, as they are the earliest known representatives of modern salamander groups, and thus, provide important insights into the early evolution of some anatomical structures and the biogeographic history of these tailed amphibians. Living salamanders form China have been grouped in three families: the Hynobiidae, the Cryptobranchidae, and the Salamandridae. None of the fossil salamanders reported from northern China can be assigned to any of these families except for one taxon, Chunerpeton, which is referred to the Cryptobranchidae. Laccotriton subsolanus (Fig. 109) is the first Mesozoic salamander reported from China. It is a small-sized metamorphosed salamander, represented by a large number of articulated skeletons from a small quarry in Fengshan Basin of northern Hebei Province. Laccotriton subsolanus is characterized by having 16 presacrals and unicapitate ribs with a broadened base (most living salamanders have bicapitate ribs, except for hynobiids and cryptobranchids). It primitively retains lacrimal and prefrontal bones on the skull, and has five separate bones in the lower jaw. The phalangeal formula (number of phalanges in hand and foot) is in the hands, and in the feet. Sinerpeton fengshanensis (Fig. 110) is another salamander from the Fengshan site, and the fossils were collected from the same quarry as that of Laccotriton. Different from the metamorphosed Laccotriton, this salamander has ossified ceratobranchials (as bony support for external gill filaments in life) and ossified carpals and tarsals (ossification of these bones only seen in adulthood). The combination of these features suggests a mature individual with larval external gills, a condition called neoteny in modern biology. Sinerpeton also differs from Laccotriton in having the phalangeal formula of in the hands and in the feet. Jeholotriton paradoxus (Figs. 111, 112) is reported from the Daohugou locality, Ningcheng County, Inner Mongolia. This apparently is an aquatic salamander as indicated by its external gills, laterally compressed tail, presence of well-developed haemal arches on caudal vertebrae, and the lack of ossified carpal and tarsal elements. Jeholotriton is a special Mesozoic salamander showing a combination of larval and adult features that indicate neoteny. The larval features include the presence of external gills, a tooth-bearing coronoid bone on the lower jaw, the larval shaped pterygoids and a short maxillary arcade with underdeveloped maxilla in the cranial part. The adult features include extensive medial contact of the two nasals and the presence of a posteriorly directed tooth row in the palate. Jeholotriton is characterized by having 17 presacrals, the vertebrae with short transverse processes, and a prominent dorsal process on the premaxillae. Its
4 ribs are like those of Fengshan salamanders as unicapitate and proximally expanded. The phalangeal formula is for the hands and for the feet. Chunerpeton tianyiensis (Fig. 113) is another salamander from the Daohugou site. This salamander represents a basal member of the Cryptobranchidae, the family including the endangered Asian giant salamander Andrias (Fig. 114, Upper) and the North American hellbender Cryptobranchus. Morphologically, Chunerpeton shares with extant cryptobranchids several derived characters, such as the nasals being much narrower than the interorbital width; nasal-prefrontal contact absent; and the anterolateral process of parietal extending along the lateral border of the frontal. It primarily differs from extant cryptobranchids, however, in lacking the frontal-maxillary contact; retention of a palatal fenestra between vomers; presence of a distinct medial process of pterygoid; and ossification of basibranchial II as a trident-shaped structure. Because no pre-paleocene fossils were known for the family, the Chunerpeton fossils from the Daohugou site document the first Mesozoic and the earliest known record of the Cryptobranchidae. The fossils also provide evidence supporting the hypothesis that the divergence of the Cryptobranchidae from the Hynobiidae had taken place during the Jurassic in Asia. Liaoxitriton zhongjiani (Fig. 115) is the only salamander taxon of the Jehol Biota that is known from the Jiufotang Formation. Fossils of this salamander were recovered from a site near Huludao City of western Liaoning. As the formation is dated as about 110 million years BP, Liaoxitriton documents so far the youngest stratigraphic occurrence of salamander fossils in the Jehol Group. The species is represented by dozens of articulated skeletons in various preservation conditions, and was the first Chinese Mesozoic lissamphibian to be reported with well-preserved soft tissue impressions (e.g., the skin & eye impressions). The diagnostic features of this animal include the presence of 16 presacral vertebrae and transverse processes of vertebra about half-length of the centrum. It also has the cryptobranchoid type unicapitate ribs with an expanded proximal end. The phalangeal formula is in the hands and in the feet. This salamander is similar to some living hynobiids (Fig. 114, Lower) in several osteological features. It is noted that the species is represented by a series of fossils showing different developmental stages, which allows a possible ontogenetic study of the animal in the near future. In general, the amphibian fossils (especially those of salamanders) from the Mesozoic beds in northern China are important for their superb preservation, large quantity, and considerable taxonomic diversity. The discoveries of these wonderful fossils provide solid paleontological evidence to answer some major questions on the evolution of amphibians; and the studies of these fossils have opened a new window to view the evolutionary history, including the origins, taxonomic diversification and geographic radiation, of modern amphibians. Figure Legends Fig. 104 Fig. 105 Fig. 106 Holotype of Callobatrachus sanyanensis (snout-pelvis length 94 mm), a discoglossid frog, from Sihetun locality (lower part of Yixian Formation, Early Cretaceous) in Beipiao, Liaoning. (Photo: IVPP) Skeletal reconstruction of Callobatrachus sanyanensis. 1, sacrum; 2, presacral vertebrae; 3, urostyle; 4, ilium. (Art: Yuan Wang/ IVPP) Bombina orientalis, a living discoglossid frog mainly distributed in East Asia, and
5 an extant relative of Callobatrachus. (Courtesy: Er-mi Zhao/ CIB) Fig. 107 Fig. 108 Holotype of Mesophryne beipiaoensis (Slab A, dorsal view, snout-pelvis length about 71 mm), a primitive frog representing a distinct basal anuran clade, from Heitizigou locality (lower part of Yixian Formation) in Beipiao, Liaoning. (Photo: IVPP) Cladogram showing the hypothesized phylogenetic relationships of major lineages of archaic anurans and the relationships within the Discoglossidae, with two Jehol frogs included (in red). Fig. 109 A specimen of Laccotriton subsolanus (dorsal view, snout-pelvis length about 40 mm), a small, primitive metamorphic salamander, from Fengshan locality in Fengning, Hebei. (Photo: Mick Ellison/ AMNH) Fig. 110 Holotype of Sinerpeton fengshanensis (dorsal view, snout-pelvis length 47 mm), a primitive salamander with neotenic features indicated by the ossified ceratobranchial (denoted by a red arrow) and ossified carpals and tarsals (denoted by yellow arrows), from Fengshan locality in Fengning, Hebei. (Photo: Mick Ellison/ AMNH) Fig. 111 Holotype of Jeholotriton paradoxus (Slab A, ventral view, body length about 140 mm), a primitive neotenic salamander similar to living cryptobranchoids in some skeletal structures, from Daohugou locality in Ningcheng, Inner Mongolia. (Photo: IVPP) Fig. 112 One of the three paratypes of Jeholotriton paradoxus (Slab A, lateral view). Note aquatic adaptation as shown by the presence of external gills (denoted by a red arrow), laterally compressed tail, unossified carpals and tarsals, and some other osteological features. (Photo: IVPP) Fig. 113 Holotype of Chunerpeton tianyiensis (part and counterpart, body length about 180 mm), a basal cryptobranchid salamander and the only Mesozoic member of the group found to date, from Daohugou locality near Ningcheng, Inner Mongolia. (Photo: Mick Ellison/ AMNH) Fig. 114 Batrachuperus pinchonii (Upper) and Andrias davidianus (Lower), a living representative of the Hynobiidae and Cryptobranchidae, respectively; the two families are widely accepted as the most basal groups of living salamanders. (Courtesy: Er-mi Zhao/ CIB) Fig. 115 Holotype of Liaoxitriton zhongjiani (Slab A, ventral view, body length about 120 mm), a primitive salamander similar to living hynobiids in some skeletal structures, from Shuikouzi locality (Jiufotang Formation) in Huludao, Liaoning. (Photo: IVPP)
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